Paty was killed outside his school near Paris on October 16, 2020, by an 18-year-old Russian of Chechen origin, who was shot to death by police.
Those on trial include friends of assailant Abdoullakh Anzorov who allegedly helped buy weapons for the attack, as well as people who are accused of spreading false information online about the teacher and his class.
The proceedings began under high security on Monday in the presence of members of Paty's family, including his two sisters.
Five of the accused, who are currently imprisoned, were seated in a wide glass box.
Three others, placed under judicial supervision, sat on the defendants' benches.
The attack occurred against a backdrop of protests in many Muslim countries and calls online for violence targeting France and the satirical French newspaper Charlie Hebdo.
The newspaper had republished its caricatures of the Prophet Mohammed a few weeks before Paty's death to mark the opening of the trial over deadly 2015 attacks on its newsroom by Islamic extremists.
The cartoon images deeply offended many Muslims, who saw them as sacrilegious.
But the fallout from Paty's killing reinforced the French state's commitment to freedom of expression and its firm attachment to secularism in public life.
Much attention will focus on Brahim Chnina, the Muslim father of a teenager who was 13 at the time and claimed she had been excluded from Paty's class when he showed the caricatures on October 5, 2020.
Chnina, 52, sent messages to his contacts denouncing Paty, saying "this sick man" needed to be fired, along with the address of the Paris school.
In reality, Chnina's daughter had lied to him and had never attended the lesson in question.
Paty was giving a lesson mandated by the education ministry, and discussed the caricatures in this context, saying students who did not wish to see them could temporarily leave the classroom.
An online campaign against Paty snowballed, and 11 days after the lesson, Anzorov attacked the teacher with a knife as he walked home, and displayed the teacher's head on social media.
Police later shot Anzorov as he advanced towards them armed.
Chnina will be tried for alleged association with a terrorist enterprise for targeting the 47-year-old teacher through false information.
His daughter was tried in 2023 in a juvenile court and given an 18-month suspended sentence.
Five other students at Paty's school were found guilty of involvement and given suspended sentences.
